Elsevier

Behavioural Brain Research

Volume 355, 14 December 2018, Pages 24-35
Behavioural Brain Research

Research report
Error blindness and motivational significance: Shifts in networks centering on anterior insula co-vary with error awareness and pupil dilation

https://doi.org/10.1016/j.bbr.2017.10.030Get rights and content

Abstract

This investigation aims to further our understanding of the brain mechanisms underlying the awareness of one’s erroneous actions. While all errors are registered as such in the rostral cingulate zone, errors enter awareness only when the anterior insula cortex is activated. Aware but not unaware errors elicit autonomic nervous system reactivity. Our aim is to investigate the hypothesis that activation in the insula during error awareness is related to autonomic arousal and to inter-regional interactions with other areas of the brain. To examine the role of the anterior insula in error awareness, we assessed its functional connectivity to other brain regions along with autonomic nervous system reactivity in young healthy participants who underwent simultaneous pupil-diameter and functional magnetic resonance imaging measurements while performing a complex and error-prone task. Error blindness was associated with failures to engage sufficient autonomic reactivity. During aware errors increased pupil-diameter along with increased task-related activation within, and increased connectivity between anterior insula and task-related networks suggested an increased capacity for action-control information transfer. Increased pupil-diameter during aware errors was furthermore associated with decreased activation of the default-mode network along with decreased insular connectivity with regions of the default mode system, possibly reflecting decreased task-irrelevant information processing. This shifting mechanism may be relevant to a better understanding of how the brain and the autonomic nervous system interact to enable efficient adaptive behavior during cognitive challenge

Introduction

Here we seek to understand the brain- and autonomic mechanisms underlying the awareness of one’s erroneous actions. The relevance of insight into the conditions under which error awareness arises is probably most readily apparent in pathologic conditions that are associated with deficits in error awareness. Deficits in error awareness occur in health as well as in pathology. Impaired error processing abilities have for instance been suggested to mediate poor insight in one’s deficits after traumatic brain injury [33], [51]. This represents a key obstacle to rehabilitation, and is a significant predictor for overall long-term outcome, return to community living, and productive lifestyle (see for a review [42]).

The recent literature in the field of error awareness can be characterized by an increasing attempt to explore mechanisms and conditions under which error awareness occurs. The anterior insula cortex has been found to activate selectively to aware errors, whereas the rostral cingulate zone shows no difference between unaware and aware errors [34], [41]. However, during error awareness, the insula’s variety of operating characteristics within several contexts, such as autonomic processes [15], [16], interoception [10], visceral sensory and motor processes, limbic integration [3], and large-scale brain network shifts [45], [60], [62], has yet prevented a clear distinction of its precise functional contributions to error awareness. Limited data is available on the networks of the human insula cortex, and reports on arousal signals mediating insula networks are largely lacking.

By articulating the insula’s functional network and autonomic function, we aim to gain more insight into the nature of the insula’s activity during error awareness. This approach was specifically motivated by the observation that the insula cortex plays a principal role in error awareness, in the mapping of autonomic and visceral functions [12], and is involved in neural networks dedicated to the evaluation of motivational salience [60], [62]. Moreover, several studies place increasing emphasis on the changes in the autonomic nervous system during error awareness (e.g., [50], [71]). Traditionally, the use of terms like vegetative or involuntary to describe the function of the autonomic nervous system implied that the autonomic nervous system has little to do with cognitive or voluntary actions. However, studies of autonomic activity that accompanies attention, cognitive effort, and the orienting to surprising events, have demonstrated that the autonomic nervous system is not simply a ‘non-cognitive’ part of brain function [35]. Autonomic arousal is commonly thought to prepare the organism to respond to changed internal and external requirements, by recruiting the necessary mental as well as physical effort [57], [68].

One index of autonomic arousal is pupil dilation. Pupil diameter constitutes an indirect index for the tonic and phasic modes of locus coeruleus-norepinephrine (LC/NE) function [56], that can be linked to lapses of task engagement and poorer performance [29]. In monkeys, the firing of LC/NE neurons is followed immediately by pupil dilation [37], in particular in relation to the energization of behavior [69]. Within cognitive tasks, baseline pupil diameter (just preceding a task-relevant stimulus) and evoked pupil dilation (following the stimulus) can serve as indices for tonic and phasic modes of LC/NE function, respectively [1], [47]. While small baseline pupil diameter and large task-evoked dilations have been proposed to correspond to effortful task engagement, task disengagement has been associated with large baseline diameter and small task-evoked dilations [29]. In line with these findings, pupil dilation has been shown to increase after aware errors, but not after unaware errors [71]. These findings on LC/NE function and pupil dilation emphasize the link between autonomic function and cognition.

In recent years, researchers have begun to investigate the link between brain function and autonomic function during cognitive operations. Although intriguing, thus far these new studies leave open the question to what extent autonomic signals during cognitive operations are related to brain function during error awareness, and to inter-regional brain network communication.

Here, in order to capture the relation between error awareness, autonomic activity and neural network activation and connectivity, participants performed an antisaccade task, known to yield both aware and unaware errors [25], [41], [49], while undergoing simultaneous fMRI, oculomotor and pupil diameter measurements. We quantify anterior insula’s functional activation and functional connectivity and its relation to changes in pupil diameter one second before error awareness. The aim is to investigate the hypothesis that activation in the insula during error awareness is related to autonomic arousal and to inter-regional interactions with other areas of the brain. We examine moreover if these inter-regional interactions of the insula cortex during error awareness are mediated by autonomic arousal. We hypothesized that pupillary responses before error awareness are related to activity in the anterior insula and its related functional networks. Although such a link cannot disentangle whether the pupil response and the anterior insula networks serve as precursors or as sequelae to awareness of an error, such a link would yield evidence that a crucial function of the anterior insula is to integrate homeostatic regulation and neural network functions once an error has been detected.

Section snippets

Participants

23 healthy right-handed volunteers (17 females, mean age 21,5±2,0) with normal or corrected-to-normal vision participated in the experiment after giving written informed consent according to the Helsinki Declaration. They were paid 50 Euros for participation. None of the participants had a history of neurological or psychiatric disorders or eye problems, and none were taking medication influencing the central nervous system or cardiovascular systems. Participants were selected beforehand in a

Behavioral results

The mean error rate was 28.1 ± 13.7% (s.d.), and the majority of errors were made on trials with a precue (80.2 ± 15.0%). Pair-wise comparisons indicated that aware errors and unaware errors occurred equally often (13.5 ± 10.4% vs. 14.6 ± 8.7%; t(22) = 0.43; p = 0.67; see Fig. 1b), and there was no significant difference between the occurrence of aware or unaware errors on precue trials (81.9 ± 17.1% vs 73.5 ± 23.6%; t(22) = 1.53; p = 0.14). Unaware errors were corrected significantly more

Discussion

The goal of the current study was to capture the relationship between states of error awareness and patterns of activation and connectivity in neural networks centering on the anterior insula in relation to autonomic activity while participants performed the antisaccade task. To date, pupil diameter changes during cognitive control tasks have scarcely been addressed in studies of functional brain connectivity (for a recent example see [24]. Therefore, for a thorough understanding of the

Conclusion

To conclude, the current data provide a direct link between the awareness state, the neural activity and connectivity of insular cortex, and the associated variability in peripheral autonomic response measures. Anterior insula networks shifted between task-related brain structures and default mode systems and co-varied with the physiological arousal system. These results advance our understanding of anterior insula network function and of dissociations between aware and unaware processing.

References (73)

  • K. Hugdahl

    Cognitive influences on human autonomic nervous system function?

    Curr. Opin. Neurobiol.

    (1996)
  • S. Joshi et al.

    Relationships between pupil diameter and neuronal activity in the locus coeruleus colliculi, and cingulate cortex

    Neuron

    (2016)
  • A.M. Kelly et al.

    Competition between functional brain networks mediates behavioral variability

    Neuroimage

    (2008)
  • T.A. Klein et al.

    Neural correlates of error awareness

    Neuroimage

    (2007)
  • J.C. Mazziotta et al.

    A probabilistic atlas of the human brain: theory and rationale for its development. The International Consortium for Brain Mapping (ICBM)

    Neuroimage

    (1995)
  • R.G. O'Connell et al.

    The neural correlates of deficient error awareness in attention-deficit hyperactivity disorder (ADHD)

    Neuropsychologia

    (2009)
  • F.M. O'Keeffe et al.

    Poor insight in traumatic brain injury mediated by impaired error processing? Evidence from electrodermal activity

    Brain Res. Cogn. Brain Res.

    (2004)
  • K.R. Ridderinkhof

    Neurocognitive mechanisms of perception-action coordination: a review and theoretical integration

    Neurosci. Biobehav. Rev.

    (2014)
  • L. Tian et al.

    Enhanced resting[HYPHEN]state brain activities in ADHD patients: a fMRI study

    Brain Develop.

    (2008)
  • L.Q. Uddin et al.

    The anterior insula in autism: under-connected and under-examined

    Neurosci. Biobehav. Rev.

    (2009)
  • G. Aston-Jones et al.

    An integrative theory of locus coeruleus-norepinephrine function: adaptive gain and optimal performance

    Annu. Rev. Neurosci.

    (2005)
  • G. Aston-Jones et al.

    Locus coeruleus neurons in monkey are selectively activated by attended cues in a vigilance task

    J. Neurosci.

    (1994)
  • M.W. Chee et al.

    Lapsing during sleep deprivation is associated with distributed changes in brain activation

    J. Neurosci.

    (2008)
  • A.D. Craig

    How do you feel?: Interoception: the sense of the physiological condition of the body

    Nat. Rev. Neurosci.

    (2002)
  • A.D. Craig

    How do you feel–now? The anterior insula and human awareness

    Nat. Rev. Neurosci.

    (2009)
  • A.D. Craig

    Significance of the insula for the evolution of human awareness of feelings from the body

    Ann. N. Y. Acad. Sci.

    (2011)
  • H.D. Critchley

    The human cortex responds to an interoceptive challenge

    Proc. Nat. Acad. Sci. U. S. A.

    (2004)
  • H.D. Critchley

    Neural mechanisms of autonomic, affective: and cognitive integration

    J. Comp. Neurol.

    (2005)
  • H.D. Critchley et al.

    Neuroanatomical basis for first- and second-order representations of bodily states

    Nat. Neurosci.

    (2001)
  • H.D. Critchley et al.

    Neural systems supporting interoceptive awareness

    Nat. Neurosci.

    (2004)
  • M. Czisch et al.

    Decision-related pupil dilation reflects upcoming choice and individual bias

    Proc. Natl. Acad. Sci. U. S. A.

    (2014)
  • A. Di Martino et al.

    Relationship between cingulo-insular functional connectivity and autistic traits in neurotypical adults

    Am. J. Psychiatry

    (2009)
  • N.U. Dosenbach et al.

    Distinct brain networks for adaptive and stable task control in humans

    Proc. Nat. Acad. Sci. U. S. A.

    (2007)
  • T. Eichele et al.

    Prediction of human errors by maladaptive changes in event-related brain networks

    Proc. Nat. Acad. Sci. U. S. A.

    (2008)
  • E. Eldar et al.

    The effects of neural gain on attention and learning

    Nat. Neurosci.

    (2013)
  • T. Endrass et al.

    ERP correlates of conscious error recognition: aware and unaware errors in an antisaccade task

    Eur. J. Neurosci.

    (2007)
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